Effects of stimulation of soluble guanylate cyclase on diabetic nephropathy in diabetic eNOS knockout mice on top of angiotensin II receptor blockade

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Ott, Ina M ^a,b   Alter, Markus L ^b,c   von Websky, Karoline ^a,b   Kretschmer, Axel ^d   Tsuprykov, Oleg ^a,b   Sharkovska, Yuliya ^b   Krause Relle, Katharina ^a,b   Raila, Jens ^a   Henze, Andrea ^a   Stasch, Johannes Peter ^d,e   Hocher, Berthold ^a,b  

^a UNIVERSITY OF POTSDAM   (Germany)

^b DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d BAYER PHARMA AG   (Germany)

^e MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; ANGIOTENSIN RECEPTOR; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE; GUANYLATE CYCLASE; MALONALDEHYDE; MONOCYTE CHEMOTACTIC PROTEIN 1; RIOCIGUAT; STREPTOZOCIN; TELMISARTAN; TUMOR NECROSIS FACTOR ALPHA;

ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE REGULATION; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC NEPHROPATHY; ENZYME ACTIVATION; GLUCOSE BLOOD LEVEL; IMMUNOREACTIVITY; KIDNEY MASS; KNOCKOUT MOUSE; LIVER WEIGHT; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; RECEPTOR BLOCKING; STREPTOZOCIN DIABETES; TREATMENT DURATION; TREATMENT OUTCOME;

ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; BENZIMIDAZOLES; BENZOATES; BIOLOGICAL MARKERS; BLOOD GLUCOSE; BLOOD PRESSURE; DIABETIC NEPHROPATHIES; DISEASE MODELS, ANIMAL; GUANYLATE CYCLASE; KIDNEY FUNCTION TESTS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE SYNTHASE TYPE III; ORGAN SIZE; PYRAZOLES; PYRIMIDINES; RECEPTORS, ANGIOTENSIN; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 84865025608     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042623     Document Type: Article

References (57)

1. Gray SP, Cooper ME, (2011) Diabetic nephropathy in 2010: Alleviating the burden of diabetic nephropathy. Nat Rev Nephrol 7: 71-73.
2. van Dieren S, Beulens JW, van der Schouw YT, Grobbee DE, Neal B, (2010) The global burden of diabetes and its complications: an emerging pandemic. Eur J Cardiovasc Prev Rehabil 17 Suppl 1: S3-8.
3. Zimmet P, Alberti KG, Shaw J, (2001) Global and societal implications of the diabetes epidemic. Nature 414: 782-787.
4. Mann JF, Schmieder RE, McQueen M, Dyal L, Schumacher H, et al. (2008) Renal outcomes with telmisartan, ramipril, or both, in people at high vascular risk (the ONTARGET study): a multicentre, randomised, double-blind, controlled trial. Lancet 372: 547-553.
5. Yusuf S, Teo KK, Pogue J, Dyal L, Copland I, et al. (2008) Telmisartan, ramipril, or both in patients at high risk for vascular events. N Engl J Med 358: 1547-1559.
6. Higashi Y, Sasaki S, Nakagawa K, Ueda T, Yoshimizu A, et al. (2000) A comparison of angiotensin-converting enzyme inhibitors, calcium antagonists, beta-blockers and diuretic agents on reactive hyperemia in patients with essential hypertension: a multicenter study. J Am Coll Cardiol 35: 284-291.
7. Jandeleit-Dahm KA, Tikellis C, Reid CM, Johnston CI, Cooper ME, (2005) Why blockade of the renin-angiotensin system reduces the incidence of new-onset diabetes. J Hypertens 23: 463-473.
8. Makino H, Haneda M, Babazono T, Moriya T, Ito S, et al. (2007) Prevention of transition from incipient to overt nephropathy with telmisartan in patients with type 2 diabetes. Diabetes Care 30: 1577-1578.
9. Schmieder RE, Delles C, Mimran A, Fauvel JP, Ruilope LM, (2007) Impact of telmisartan versus ramipril on renal endothelial function in patients with hypertension and type 2 diabetes. Diabetes Care 30: 1351-1356.
10. Brosius FC 3rd, Alpers CE, Bottinger EP, Breyer MD, Coffman TM, et al. (2009) Mouse models of diabetic nephropathy. J Am Soc Nephrol 20: 2503-2512.
11. Kanetsuna Y, Takahashi K, Nagata M, Gannon MA, Breyer MD, et al. (2007) Deficiency of endothelial nitric-oxide synthase confers susceptibility to diabetic nephropathy in nephropathy-resistant inbred mice. Am J Pathol 170: 1473-1484.
12. Nakagawa T, Sato W, Glushakova O, Heinig M, Clarke T, et al. (2007) Diabetic endothelial nitric oxide synthase knockout mice develop advanced diabetic nephropathy. J Am Soc Nephrol 18: 539-550.
13. Brosius FC 3rd, (2008) New insights into the mechanisms of fibrosis and sclerosis in diabetic nephropathy. Rev Endocr Metab Disord 9: 245-254.
14. Futrakul N, Butthep P, Vongthavarawat V, Futrakul P, Sirisalipoch S, et al. (2006) Early detection of endothelial injury and dysfunction in conjunction with correction of hemodynamic maladjustment can effectively restore renal function in type 2 diabetic nephropathy. Clin Hemorheol Microcirc 34: 373-381.
15. Stasch JP, Pacher P, Evgenov OV, (2011) Soluble guanylate cyclase as an emerging therapeutic target in cardiopulmonary disease. Circulation 123: 2263-2273.
16. Schermuly RT, Stasch JP, Pullamsetti SS, Middendorff R, Muller D, et al. (2008) Expression and function of soluble guanylate cyclase in pulmonary arterial hypertension. Eur Respir J 32: 881-891.
17. Sharkovska Y, Kalk P, Lawrenz B, Godes M, Hoffmann LS, et al. (2010) Nitric oxide-independent stimulation of soluble guanylate cyclase reduces organ damage in experimental low-renin and high-renin models. J Hypertens 28: 1666-1675.
18. Geschka S, Kretschmer A, Sharkovska Y, Evgenov OV, Lawrenz B, et al. (2011) Soluble guanylate cyclase stimulation prevents fibrotic tissue remodeling and improves survival in salt-sensitive Dahl rats. PLoS One 6: e21853.
19. Mittendorf J, Weigand S, Alonso-Alija C, Bischoff E, Feurer A, et al. (2009) Discovery of riociguat (BAY 63-2521): a potent, oral stimulator of soluble guanylate cyclase for the treatment of pulmonary hypertension. ChemMedChem 4: 853-865.
20. Haffner D, Hocher B, Muller D, Simon K, Konig K, et al. (2005) Systemic cardiovascular disease in uremic rats induced by 1,25(OH)2D3. J Hypertens 23: 1067-1075.
21. Hocher B, George I, Diekmann F, Zart R, Rebstock J, et al. (2000) ETA receptor blockade induces fibrosis of the clipped kidney in two-kidney-one-clip renovascular hypertensive rats. J Hypertens 18: 1807-1814.
22. Tomson C, Udayaraj U, Gilg J, Ansell D, (2007) Comorbidities in UK patients at the start of renal replacement therapy (chapter 6). Nephrol Dial Transplant 22 Suppl 7: vii58-68.
23. Nakayama M, Yasue H, Yoshimura M, Shimasaki Y, Kugiyama K, et al. (1999) T-786→C mutation in the 5′-flanking region of the endothelial nitric oxide synthase gene is associated with coronary spasm. Circulation 99: 2864-2870.
24. Tsukada T, Yokoyama K, Arai T, Takemoto F, Hara S, et al. (1998) Evidence of association of the ecNOS gene polymorphism with plasma NO metabolite levels in humans. Biochem Biophys Res Commun 245: 190-193.
25. Veldman BA, Spiering W, Doevendans PA, Vervoort G, Kroon AA, et al. (2002) The Glu298Asp polymorphism of the NOS 3 gene as a determinant of the baseline production of nitric oxide. J Hypertens 20: 2023-2027.
26. Zanchi A, Moczulski DK, Hanna LS, Wantman M, Warram JH, et al. (2000) Risk of advanced diabetic nephropathy in type 1 diabetes is associated with endothelial nitric oxide synthase gene polymorphism. Kidney Int 57: 405-413.
27. Ezzidi I, Mtiraoui N, Mohamed MB, Mahjoub T, Kacem M, et al. (2008) Association of endothelial nitric oxide synthase Glu298Asp, 4b/a, and -786T>C gene variants with diabetic nephropathy. J Diabetes Complications 22: 331-338.
28. Kosugi T, Heinig M, Nakayama T, Matsuo S, Nakagawa T, (2010) eNOS knockout mice with advanced diabetic nephropathy have less benefit from renin-angiotensin blockade than from aldosterone receptor antagonists. Am J Pathol 176: 619-629.
29. Ritz E, Schmieder RE, Pollock CA, (2010) Renal protection in diabetes: lessons from ONTARGET. Cardiovasc Diabetol 9: 60.
30. Ladeia AM, Ladeia-Frota C, Pinho L, Stefanelli E, Adan L, (2005) Endothelial dysfunction is correlated with microalbuminuria in children with short-duration type 1 diabetes. Diabetes Care 28: 2048-2050.
31. Iseki K, Ikemiya Y, Iseki C, Takishita S, (2003) Proteinuria and the risk of developing end-stage renal disease. Kidney Int 63: 1468-1474.
32. Arnlov J, Evans JC, Meigs JB, Wang TJ, Fox CS, et al. (2005) Low-grade albuminuria and incidence of cardiovascular disease events in nonhypertensive and nondiabetic individuals: the Framingham Heart Study. Circulation 112: 969-975.
33. Hillege HL, Fidler V, Diercks GF, van Gilst WH, de Zeeuw D, et al. (2002) Urinary albumin excretion predicts cardiovascular and noncardiovascular mortality in general population. Circulation 106: 1777-1782.
34. Mauer SM, Steffes MW, Ellis EN, Sutherland DE, Brown DM, et al. (1984) Structural-functional relationships in diabetic nephropathy. J Clin Invest 74: 1143-1155.
35. Zatz R, Dunn BR, Meyer TW, Anderson S, Rennke HG, et al. (1986) Prevention of diabetic glomerulopathy by pharmacological amelioration of glomerular capillary hypertension. J Clin Invest 77: 1925-1930.
36. Dronavalli S, Duka I, Bakris GL, (2008) The pathogenesis of diabetic nephropathy. Nat Clin Pract Endocrinol Metab 4: 444-452.
37. Chen S, Hong SW, Iglesias-de la Cruz MC, Isono M, Casaretto A, et al. (2001) The key role of the transforming growth factor-beta system in the pathogenesis of diabetic nephropathy. Ren Fail 23: 471-481.
38. Clausell N, Kalil P, Biolo A, Molossi S, Azevedo M, (1999) Increased expression of tumor necrosis factor-alpha in diabetic macrovasculopathy. Cardiovasc Pathol 8: 145-151.
39. Masuyama H, Tsuruda T, Kato J, Imamura T, Asada Y, et al. (2006) Soluble guanylate cyclase stimulation on cardiovascular remodeling in angiotensin II-induced hypertensive rats. Hypertension 48: 972-978.
40. Masuyama H, Tsuruda T, Sekita Y, Hatakeyama K, Imamura T, et al. (2009) Pressure-independent effects of pharmacological stimulation of soluble guanylate cyclase on fibrosis in pressure-overloaded rat heart. Hypertens Res 32: 597-603.
41. Jones ES, Kemp-Harper BK, Stasch JP, Schmidt HW, Widdop RE, (2009) Cardioprotective effects in aged spontaneously hypertensive rats due to chronic stimulation/activation of sGC without hypotension. BMC Pharmacology Suppl 1pp. P29.
42. Benz K, Orth SR, Simonaviciene A, Linz W, Schindler U, et al. (2007) Blood pressure-independent effect of long-term treatment with the soluble heme-independent guanylyl cyclase activator HMR1766 on progression in a model of noninflammatory chronic renal damage. Kidney Blood Press Res 30: 224-233.
43. Peters H, Daig U, Martini S, Ruckert M, Schaper F, et al. (2003) NO mediates antifibrotic actions of L-arginine supplementation following induction of anti-thy1 glomerulonephritis. Kidney Int 64: 509-518.
44. Peters H, Wang Y, Loof T, Martini S, Kron S, et al. (2004) Expression and activity of soluble guanylate cyclase in injury and repair of anti-thy1 glomerulonephritis. Kidney Int 66: 2224-2236.
45. Hohenstein B, Daniel C, Wagner A, Stasch JP, Hugo C, (2005) Stimulation of soluble guanylyl cyclase inhibits mesangial cell proliferation and matrix accumulation in experimental glomerulonephritis. Am J Physiol Renal Physiol 288: F685-693.
46. Wang Y, Kramer S, Loof T, Martini S, Kron S, et al. (2005) Stimulation of soluble guanylate cyclase slows progression in anti-thy1-induced chronic glomerulosclerosis. Kidney Int 68: 47-61.
47. Wang Y, Kramer S, Loof T, Martini S, Kron S, et al. (2006) Enhancing cGMP in experimental progressive renal fibrosis: soluble guanylate cyclase stimulation vs. phosphodiesterase inhibition. Am J Physiol Renal Physiol 290: F167-176.
48. Stasch JP, Becker EM, Alonso-Alija C, Apeler H, Dembowsky K, et al. (2001) NO-independent regulatory site on soluble guanylate cyclase. Nature 410: 212-215.
49. Stasch JP, Dembowsky K, Perzborn E, Stahl E, Schramm M, (2002) Cardiovascular actions of a novel NO-independent guanylyl cyclase stimulator, BAY 41-8543: in vivo studies. Br J Pharmacol 135: 344-355.
50. Zanfolin M, Faro R, Araujo EG, Guaraldo AM, Antunes E, et al. (2006) Protective effects of BAY 41-2272 (sGC stimulator) on hypertension, heart, and cardiomyocyte hypertrophy induced by chronic L-NAME treatment in rats. J Cardiovasc Pharmacol 47: 391-395.
51. Del Rio D, Stewart AJ, Pellegrini N, (2005) A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardiovasc Dis 15: 316-328.
52. Onozato ML, Tojo A, Goto A, Fujita T, Wilcox CS, (2002) Oxidative stress and nitric oxide synthase in rat diabetic nephropathy: effects of ACEI and ARB. Kidney Int 61: 186-194.
53. Suzuki D, Miyata T, Saotome N, Horie K, Inagi R, et al. (1999) Immunohistochemical evidence for an increased oxidative stress and carbonyl modification of proteins in diabetic glomerular lesions. J Am Soc Nephrol 10: 822-832.
54. Horie K, Miyata T, Maeda K, Miyata S, Sugiyama S, et al. (1997) Immunohistochemical colocalization of glycoxidation products and lipid peroxidation products in diabetic renal glomerular lesions. Implication for glycoxidative stress in the pathogenesis of diabetic nephropathy. J Clin Invest 100: 2995-3004.
55. Conlon PJ, Fischer CA, Levesque MC, Smith SR, St Clair EW, et al. (1996) Clinical, biochemical and pathological predictors of poor response to intravenous cyclophosphamide in patients with proliferative lupus nephritis. Clin Nephrol 46: 170-175.
56. de Lind van Wijngaarden RA, Hauer HA, Wolterbeek R, Jayne DR, Gaskin G, et al. (2006) Clinical and histologic determinants of renal outcome in ANCA-associated vasculitis: A prospective analysis of 100 patients with severe renal involvement. J Am Soc Nephrol 17: 2264-2274.
57. Alexopoulos E, Stangou M, Papagianni A, Pantzaki A, Papadimitriou M, (2000) Factors influencing the course and the response to treatment in primary focal segmental glomerulosclerosis. Nephrol Dial Transplant 15: 1348-1356.